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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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HSV-1 ICP27 induces apoptosis by promoting Bax translocation to mitochondria through interacting with 14-3-3θ

  • Kim, Ji Ae (Department of Microbiology & Molecular Biology, College of Biological Science and Biotechnology, Chungnam National University) ;
  • Kim, Jin Chul (Division of Biological Sciences, University of California) ;
  • Min, Jung Sun (Department of Microbiology & Molecular Biology, College of Biological Science and Biotechnology, Chungnam National University) ;
  • Kang, Inho (Department of Microbiology & Molecular Biology, College of Biological Science and Biotechnology, Chungnam National University) ;
  • Oh, Jeongho (Department of Microbiology & Molecular Biology, College of Biological Science and Biotechnology, Chungnam National University) ;
  • Ahn, Jeong Keun (Department of Microbiology & Molecular Biology, College of Biological Science and Biotechnology, Chungnam National University)
  • Received : 2017.02.09
  • Accepted : 2017.03.03
  • Published : 2017.05.31
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Abstract

The subcellular localization of Bax plays a crucial role during apoptosis. In response to apoptotic stimuli, Bax translocates from the cytoplasm to the mitochondria, where it promotes the release of cytochrome c to the cytoplasm. In cells infected with HSV-1, apoptosis is triggered or blocked by diverse mechanisms. In this study, we demonstrate how HSV-1 ICP27 induces apoptosis and modulates mitochondrial membrane potential in HEK 293T cells. We found that ICP27 interacts with $14-3-3{\theta}$ which sequesters Bax to the cytoplasm. In addition, ICP27 promotes the translocation of Bax to the mitochondria by inhibiting the interaction between $14-3-3{\theta}$ and Bax. Our findings may provide a novel apoptotic regulatory pathway induced by ICP27 during HSV-1 infection.

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References

  1. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35, 495-516 https://doi.org/10.1080/01926230701320337
  2. Ashkenazi A and Dixit VM (1998) Death receptors: signaling and modulation. Science 281, 1305-1308 https://doi.org/10.1126/science.281.5381.1305
  3. Schmitz I, Kirchhoff S and Krammer PH (2000) Regulation of death receptor-mediated apoptosis pathways. Int J Biochem Cell Biol 32, 1123-1136 https://doi.org/10.1016/S1357-2725(00)00048-0
  4. Wang X (2001) The expanding role of mitochondria in apoptosis. Genes Dev 15, 2922-2933
  5. Cory S and Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2, 647-656 https://doi.org/10.1038/nrc883
  6. Martinou JC and Green DR (2001) Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2, 63-67
  7. Knudson CM, Tung KS, Tourtellotte WG, Brown GA and Korsmeyer SJ (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270, 96-99 https://doi.org/10.1126/science.270.5233.96
  8. Wei MC, Zong WX, Cheng EH et al (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730 https://doi.org/10.1126/science.1059108
  9. Tsuruta F, Sunayama J, Mori Y et al (2004) JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J 23, 1889-1899 https://doi.org/10.1038/sj.emboj.7600194
  10. Kuwana T, Mackey MR, Perkins G et al (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111, 331-342 https://doi.org/10.1016/S0092-8674(02)01036-X
  11. Nomura M, Shimizu S, Sugiyama T et al (2003) 14-3-3 Interacts directly with and negatively regulates proapoptotic Bax. J Biol Chem 278, 2058-2065 https://doi.org/10.1074/jbc.M207880200
  12. Honess RW and Roizman B (1974) Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. J Virol 14, 8-19
  13. Smiley JR (2004) Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase? J Virol 78, 1063-1068 https://doi.org/10.1128/JVI.78.3.1063-1068.2004
  14. Chen IH, Li L, Silva L and Sandri-Goldin RM (2005) ICP27 recruits Aly/REF but not TAP/NXF1 to herpes simplex virus type 1 transcription sites although TAP/NXF1 is required for ICP27 export. J Virol 79, 3949-3961 https://doi.org/10.1128/JVI.79.7.3949-3961.2005
  15. Song BW, Yeh KC, Liu J and Knipe DM (2001) Herpes simplex virus gene products required for viral inhibition of expression of G1-phase functions. Virology 290, 320-328 https://doi.org/10.1006/viro.2001.1175
  16. Lynn EG, McLeod CJ, Gordon JP, Bao JJ and Sack MN (2008) SIRT2 is a negative regulator of anoxia-reoxygenation tolerance via regulation of 14-3-3 zeta and BAD in H9c2 cells. FEBS Lett 582, 2857-2862 https://doi.org/10.1016/j.febslet.2008.07.016
  17. Dougherty MK and Morrison DK (2004) Unlocking the code of 14-3-3. J Cell Sci 117, 1875-1884 https://doi.org/10.1242/jcs.01171
  18. Tzivion G and Avruch J (2002) 14-3-3 proteins: Active cofactors in cellular regulation by serine/threonine phosphorylation. J Biol Chem 277, 3061-3064 https://doi.org/10.1074/jbc.R100059200
  19. Sanfilippo CM, Chirimuuta FN and Blaho JA (2004) Herpes simplex virus type 1 immediate-early gene expression is required for the induction of apoptosis in human epithelial HEp-2 cells. J Virol 78, 224-239 https://doi.org/10.1128/JVI.78.1.224-239.2004
  20. Kim JC, Choi SH, Kim JK et al (2008) Herpes simplex virus type 1 ICP27 induces apoptotic cell death by increasing intracellular reactive oxygen species. Mol Biol 42, 413-420 https://doi.org/10.1134/S0026893308030096
  21. Aubert M and Blaho JA (1999) The herpes simplex virus type 1 regulatory protein ICP27 is required for the prevention of apoptosis in infected human cells. J Virol 73, 2803-2813
  22. Aubert M, Rice SA and Blaho JA (2001) Accumulation of herpes simplex virus type 1 early and leaky-late proteins correlates with apoptosis prevention in infected human HEp-2 cells. J Virol 75, 1013-1030 https://doi.org/10.1128/JVI.75.2.1013-1030.2001
  23. Gillis PA, Okagaki LH and Rice SA (2009) Herpes simplex virus type 1 ICP27 induces p38 mitogen-activated protein kinase signaling and apoptosis in HeLa cells. J Virol 83, 1767-1777 https://doi.org/10.1128/JVI.01944-08
  24. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG and Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139, 1281-1292 https://doi.org/10.1083/jcb.139.5.1281
  25. Kuwana T, Mackey MR, Perkins G et al (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111, 331-342 https://doi.org/10.1016/S0092-8674(02)01036-X
  26. Kim HJ, Kim SY, Kim J et al (2008) Hepatitis B virus X protein induces apoptosis by enhancing translocation of Bax to mitochondria. IUBMB Life 60, 473-480 https://doi.org/10.1002/iub.68
  27. Aitken A (2011) Post-translational modification of 14-3-3 isoforms and regulation of cellular function. Semin Cell Dev Biol 22, 673-680 https://doi.org/10.1016/j.semcdb.2011.08.003
  28. Aitken A (2002) Functional specificity in 14-3-3 isoform interactions through dimer formation and phosphorylation. Chromosome location of mammalian isoforms and variants. Plant Mol Biol 50, 993-1010 https://doi.org/10.1023/A:1021261931561
  29. Kanno T and Nishizaki T (2011) Sphingosine induces apoptosis in hippocampal neurons and astrocytes by activating caspase-3/-9 via a mitochondrial pathway linked to SDK/14-3-3 protein/Bax/cytochrome c. J Cell Physiol 226, 2329-2337 https://doi.org/10.1002/jcp.22571
  30. Tsuruta F, Sunayama J, Mori Y et al (2004) JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J 23, 1889-1899 https://doi.org/10.1038/sj.emboj.7600194
  31. McMahan L and Schaffer PA (1990) The repressing and enhancing functions of the herpes simplex virus regulatory protein ICP27 map to C-terminal regions and are required to modulate viral gene expression very early in infection. J Virol 64, 3471-3485
  32. Kim JC, Lee SY, Kim SY et al (2008) HSV-1 ICP27 suppresses NF-kappaB activity by stabilizing IkappaBalpha. FEBS Lett 582, 2371-2376 https://doi.org/10.1016/j.febslet.2008.05.044
  33. Rice SA and Knipe DM (1988) Gene-Specific Transactivation by Herpes-Simplex Virus Type-1 Alpha-Protein-Icp27. J Virol 62, 3814-3823
  34. Kuo HY, Chang CC, Jeng JC et al (2005) SUMO modification negatively modulates the transcriptional activity of CREB-binding protein via the recruitment of Daxx. Proc Natl Acad Sci U S A 102, 16973-16978 https://doi.org/10.1073/pnas.0504460102
  35. Shinbo Y, Niki T, Taira T et al (2006) Proper SUMO-1 conjugation is essential to DJ-1 to exert its full activities. Cell Death Differ 13, 96-108 https://doi.org/10.1038/sj.cdd.4401704
  36. Semaan SJ and Nickells RW (2010) The apoptotic response in HCT116BAX-/- cancer cells becomes rapidly saturated with increasing expression of a GFP-BAX fusion protein. BMC Cancer 10, 554 https://doi.org/10.1186/1471-2407-10-554
  37. Abreu-Martin MT, Chari A, Palladino AA, Craft NA and Sawyers CL (1999) Mitogen-activated protein kinase kinase kinase 1 activates androgen receptor-dependent transcription and apoptosis in prostate cancer. Mol Cell Biol 19, 5143-5154 https://doi.org/10.1128/MCB.19.7.5143
  38. Miao L, Yi P, Wang Y and Wu M (2003) Etoposide upregulates Bax-enhancing tumour necrosis factor-related apoptosis inducing ligand-mediated apoptosis in the human hepatocellular carcinoma cell line QGY-7703. Eur J Biochem 270, 2721-2731 https://doi.org/10.1046/j.1432-1033.2003.03639.x
  39. Li L, Lorenzo PS, Bogi K, Blumberg PM and Yuspa SH (1999) Protein kinase Cdelta targets mitochondria, alters mitochondrial membrane potential, and induces apoptosis in normal and neoplastic keratinocytes when overexpressed by an adenoviral vector. Mol Cell Biol 19, 8547-8558 https://doi.org/10.1128/MCB.19.12.8547

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